Training Captive-Bred or Translocated Animals to Avoid Predators

Abstract: Animal reintroductions and translocations are potentially important interventions to save species from extinction, but most are unsuccessful. Mortality due to predation is a principal cause of failure. Animals that have been isolated from predators, either throughout their lifetime or over evolutionary time, may no longer express appropriate antipredator behavior. For this reason, conservation biologists are beginning to include antipredator training in pre-release preparation procedures. We describe the evolutionary and ontogenetic circumstances under which antipredator behavior may degenerate or be lost, and we use principles from learning theory to predict which elements can be enhanced or recovered by training. The empirical literature demonstrates that training can improve antipredator skills, but the effectiveness of such interventions is influenced by a number of constraints. We predict that it will be easier to teach animals to cope with predators if they have experienced ontogenetic isolation than if they have undergone evolutionary isolation. Similarly, animals should learn more easily if they have been evolutionarily isolated from some rather than all predators. Training to a novel predator may be more successful if a species has effective responses to similar predators. In contrast, it may be difficult to teach proper avoidance behavior, or to introduce specialized predator-specific responses, if appropriate motor patterns are not already present. We conclude that pre-release training has the potential to enhance the expression of preexisting antipredator behavior. Potential training techniques involve classical conditioning procedures in which animals learn that model predators are predictors of aversive events. However, wildlife managers should be aware that problems, such as the emergence of inappropriate responses, may arise during such training.     

Does information of predators influence general wariness?

Antipredator behavior includes several qualitatively distinct activities, but few studies have determined the degree to which these activities are independent. If behaviors are not independent, then the nature of the relationship would illustrate potential performance constraints. We studied crimson rosellas (Platycercus elegans) and first focused on acoustic predator discrimination. We measured time allocation before and after playback of one of three experimental treatments (peregrine falcons—Falco peregrinus, wedge-tailed eagles—Aquila audax, and crimson rosellas) to determine whether or not rosellas discriminated predators from non-predators, and specifically whether or not they discriminated large from small predators. We then focused on the decision to flee. We experimentally approached subjects and measured the distance at which they oriented to us (alert distance) and the distance at which they fled (flight initiation distance; FID). We found that rosellas could distinguish among predators; however, there was no effect on general wariness as measured by FID. These two processes of antipredator behavior may, thus, be independent.     

A case for quantile regression in behavioral ecology: getting more out of flight initiation distance data

A central goal of behavioral ecology is to quantify and explain variation in behavior. While much previous work has focused on the differences in mean behavior across groups or treatments, we present a complementary approach studying changes in the distribution of the response variable. This is important because changes in the edges of a distribution may be more informative than changes in the mean if behavior at the edges of a distribution better reflects behavioral constraints. Quantile regression estimates the rate of change of conditional quantiles of a response variable and thus allows the study of changes in any part of its distribution. Although quantile regression is gaining popularity in the ecological literature, it is strikingly unused in behavioral ecology. Here, we demonstrate the usefulness of this method by analyzing the relationship between the starting distance (SD) at which an observer approach a focal animal and its flight initiation distance (FID, the distance between the observer and the animal when it decides to flee). In particular, we used a simple model of flight initiation distance to show that in most situations ordinary least-square regression cannot be used to analyse the SD–FID relationship. Quantile regression conducted on the lowest quantiles appears more robust and we applied this approach to data from four bird species. Overall, changes in the lowest FID values appeared to be the most informative to determine if a species displays a “flush early” strategy, a strategy which has been hypothesized to be a general rule. We hope this example will bring quantile regression to the attention of behavioral ecologists as a valuable tool to add to their statistical toolbox.     

Do yellow-bellied marmots respond to predator vocalizations?

We conducted four experiments to determine whether yellow-bellied marmots, Marmota flaviventris, discriminate among predator vocalizations, and if so, whether the recognition mechanism is learned or experience-independent. First, we broadcast to marmots the social sounds of coyotes, Canis latrans, wolves, Canis lupus, and golden eagles, Aquila chrysaetos, as well as conspecific alarm calls. Coyotes and eagles are extant predators at our study site, while wolves have been absent since the mid-1930s. In three follow-up experiments, we reversed the eagle call and presented marmots with forward and reverse calls to control for response to general properties of call structure rather than those specifically associated with eagles, we tested for novelty by comparing responses to familiar and unfamiliar birds, and we tested for the duration of predator sounds by comparing a wolf howl (that was much longer than the coyote in the first experiment) with a long coyote howl of equal duration to the original wolf. Marmots suppressed foraging and increased looking most after presentation of the conspecific alarm call and least after that of the coyote in the first experiment, with moderate responses to wolf and eagle calls. Marmots responded more to the forward eagle call than the reverse call, a finding consistent with a recognition template. Marmots did not differentiate vocalizations from the novel and familiar birds, suggesting that novelty itself did not explain our results. Furthermore, marmots did not differentiate between a wolf howl and a coyote howl of equal duration, suggesting that the duration of the vocalizations played a role in the marmots’ response. Our results show that marmots may respond to predators based solely on acoustic stimuli. The response to currently novel wolf calls suggests that they have an experience-independent ability to identify certain predators acoustically. Marmots’ response to predator vocalizations is not unexpected because 25 of 30 species in which acoustic predator discrimination has been studied have a demonstrated ability to respond selectively to cues from their predators.     

Spatiotemporal variation in survival rates: implications for population dynamics of yellow-bellied marmots

Spatiotemporal variation in age-specific survival rates can profoundly influence population dynamics, but few studies of vertebrates have thoroughly investigated both spatial and temporal variability in age-specific survival rates. We used 28 years (1976-2003) of capture-mark-recapture (CMR) data from 17 locations to parameterize an age-structured Cormack-Jolly-Seber model, and investigated spatial and temporal variation in age-specific annual survival rates of yellow-bellied marmots (Marmota flaviventris). Survival rates varied both spatially and temporally, with survival of younger animals exhibiting the highest degree of variation. Juvenile survival rates varied from 0.52 +/- 0.05 to 0.78 +/- 0.10 among sites and from 0.15 +/- 0.14 to 0.89 +/- 0.06 over time. Adult survival rates varied from 0.62 +/- 0.09 to 0.80 +/- 0.03 among sites, but did not vary significantly over time. We used reverse-time CMR models to estimate the realized population growth rate (lamda), and to investigate the influence of the observed variation in age-specific survival rates on lamda. The realized growth rate of the population closely covaried with, and was significantly influenced by, spatiotemporal variation in juvenile survival rate. High variability in juvenile survival rates over space and time clearly influenced the dynamics of our study population and is also likely to be an important determinant of the spatiotemporal variation in the population dynamics of other mammals with similar life history characteristics.     

Environmental,social, morphological,and behavioral constraints on opportunistic multiple paternity

Multiple mating and multiple paternity in polytocous species have been mostly studied from an adaptive (i.e., cost–benefit) perspective. Disease, time, energy, and the risk of injuries are well-known costs of multiple mating, yet from both male and female perspectives, a number of genetic and non-genetic benefits have also been identified. The effects of environmental conditions and individual-specific behavior, however, are much less well understood. Using a long-term study on yellow-bellied marmots (Marmota flaviventris), we evaluated the impacts of environmental variation, social structure, female body mass, and female docility (a personality trait) on the occurrence of multiple paternity. Multiple paternity was influenced by environmental constraints, social constraints, a female’s personality, and her body mass at emergence from hibernation. Personality and mass effects were detected only when environmental or social conditions were favorable. Our results suggest that multiple paternity is mainly limited by the opportunity to have access to multiple mates and is influenced by costs or mate choice because heavier females were more likely to have litters with multiple sires than smaller ones. Future studies in other species might benefit from considering environmental constraints when studying multiple paternity.     

Age and sex influence marmot antipredator behavior during periods of heightened risk

Animals adjust their antipredator behavior according to environmental variation in risk, and to account for their ability to respond to threats. Intrinsic factors that influence an animal’s ability to respond to predators (e.g., age, body condition) should explain variation in antipredator behavior. For example, a juvenile might allocate more time to vigilance than an adult because mortality as a result of predation is often high for this age class; however, the relationship between age/vulnerability and antipredator behavior is not always clear or as predicted. We explored the influence of intrinsic factors on yellow-bellied marmot (Marmota flaviventris) antipredator behavior using data pooled from 4 years of experiments. We hypothesized that inherently vulnerable animals (e.g., young, males, and individuals in poor condition) would exhibit more antipredator behavior prior to and immediately following conspecific alarm calls. As expected, males and yearlings suppressed foraging more than females and adults following alarm call playbacks. In contrast to predictions, animals in better condition respond more than animals in below average condition. Interestingly, these intrinsic properties did not influence baseline time budgets; animals of all ages, sexes, and condition levels devoted comparable amounts of time to foraging prior to alarm calls. Our results support the hypothesis that inherent differences in vulnerability influence antipredator behavior; furthermore, it appears that a crucial, but poorly acknowledged, interaction exists between risk and state-dependence. Elevated risk may be required to reveal the workings of state-dependent behavior, and studies of antipredator behavior in a single context may draw incomplete conclusions about age- or sex-specific strategies.     

Social attributes and associated performance measures in marmots: bigger male bullies and weakly affiliating females have higher annual reproductive success

Studying the structure of social interactions is fundamental in behavioral ecology as social behavior often influences fitness and thus natural selection. However, social structure is often complex, and determining the most appropriate measures of variation in social behavior among individuals can be difficult. Social network analysis generates numerous, but often correlated, measures of individual connectedness derived from a network of interactions. We used measures of individual connectedness in networks of affiliative and agonistic interactions in yellow-bellied marmots, Marmota flaviventris, to first determine how variance was structured among network measures. Principal component analysis reduced our set of network measures to four “social attributes” (unweighted connectedness, affiliation strength, victimization, and bullying), which revealed differences between patterns of affiliative and agonistic interactions. We then used these extracted social attributes to examine the relationship between an individual’s social attributes and several performance measures: annual reproductive success, parasite infection, and basal stress. In male marmots, bullying was positively associated with annual reproductive success, while in females, affiliation strength was negatively associated with annual reproductive success. No other social attributes were significantly associated with any performance measures. Our study highlights the utility of considering multiple dimensions when measuring the structure and functional consequences of social behavior.     

The potential to encode sex,age, and individual identity in the alarm calls of three species of Marmotinae

In addition to encoding referential information and information about the sender’s motivation, mammalian alarm calls may encode information about other attributes of the sender, providing the potential for recognition among kin, mates, and neighbors. Here, we examined 96 speckled ground squirrels (Spermophilus suslicus), 100 yellow ground squirrels (Spermophilus fulvus) and 85 yellow-bellied marmots (Marmota flaviventris) to determine whether their alarm calls differed between species in their ability to encode information about the caller’s sex, age, and identity. Alarm calls were elicited by approaching individually identified animals in live-traps. We assume this experimental design modeled a naturally occurring predatory event, when receivers should acquire information about attributes of a caller from a single bout of alarm calls. In each species, variation that allows identification of the caller’s identity was greater than variation allowing identification of age or sex. We discuss these results in relation to each species’ biology and sociality.